PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Shchennikova A.V., Filyushin M.A., Kochieva E.Z. Stress memory in plants: key aspects (review). Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 3, p. 397-414.
(how to cite this article)

doi: 10.15389/agrobiology.2025.3.397eng

UDC: 631.522/.524

Acknowledgements:
Supported financially by Russian Science Foundation (grant No. 24-16-00043, stress memory of plants) and the Ministry of Science and Higher Education of the Russian Federation (effects of a combination of stressors)

 

STRESS MEMORY IN PLANTS: KEY ASPECTS (review)

A.V. Shchennikova✉, M.A. Filyushin, E.Z. Kochieva

Skryabin Institute of Bioengineering, Federal Research Center Fundamentals of Biotechnology RAS, 33/2, Leninskii prospect, Moscow, 119071 Russia, e-mail shchennikova@yandex.ru (✉ corresponding author), michel7753@mail.ru, ekochieva@yandex.ru

ORCID:
Shchennikova A.V. orcid.org/0000-0003-4175-3175
Kochieva E.Z. orcid.org/0000-0002-6091-0765
Filyushin M.A. orcid.org/0000-0003-3668-7601

Final revision received July 22, 2024
Accepted September 27, 2024

Plants are constantly exposed to the destructive effects of unfavorable environmental conditions, both abiotic and biotic. In the case of crops, this negatively affects yields. Numerous laboratory studies have focused on the effects of various stress factors on plant growth and development. The results of attempts to transfer the obtained data to field cultivation conditions indicate the presence of critical aspects of the plant-stress interaction. In this review, we consider some of these aspects. Thus, most studies are focused on the analysis of molecular responses of plants to single-factor stresses (Y. Saijo, et al., 2020). The natural environment is characterized by multifactorial effects in various combinations. Therefore, recently there has been an increasing number of publications analyzing the response of plants to two- and three-factor stress combinations of abiotic factors with abiotic (T. Obata et al., 2015; N. Suzuki et al., 2016; S.I. Zandalinas et al., 2022) and biotic (S. Rasmussen et al., 2013; N. Suzuki et al., 2014; A.R. Devireddy et al., 2020) stressors. It has been shown that the mechanism of plant response under combinatorial influence arises as a result of integration and modulation of responses to individual stress components (N. Suzuki et al., 2014), which can be neutral, antagonistic or unrelated to each other, and is often unpredictable and requires experimental confirmation (S. Rasmussen et al., 2013). Responses to abiotic and biotic factors are controlled by different, sometimes conflicting signaling pathways, which under combinatorial stress can interact and/or inhibit each other (S. Rasmussen et al., 2013; N. Suzuki et al., 2014). The quality of the plant stress response depends not only on the genotype, but also on the epigenetic regulation of the expression of the corresponding genes and the accumulation of the necessary metabolites (Z.H. Chen et al., 2020), known as “stress memory” (A. Weinhold, 2018). In the natural environment of plant growth, recurrent events of the same type and combinatorial stresses are not uncommon. The formation of reversible heritable stress memory occurs as a result of the plant experiencing a primary stress effect (priming). The plant remembers its defense reaction by introducing epigenetic changes into the genome and, when the stress is repeated, triggers the remembered reactions to the previous experience (M. Hilker et al., 2016; J. Lämke et al, 2017). A distinction is made between cis-priming, when the type of primary and repeated stresses coincides, and trans-priming, when the priming memory is triggered in response to a stimulus of a different type (M. Hilker et al., 2016; A.U. Nair et al., 2022). The set of epigenetic marks that arise after priming constitutes the plant's memory of the stressful event and is aimed at regulating the expression of specific genes (M. Hilker et al., 2016; L. Virlouvet et al., 2018; A. Nishad, A.K. Nandi, 2021; C. Jacques et al., 2021). Stress memory can be short-term (mitotically inherited) and long-term (meiotically inherited) (M. Hilker et al., 2016; J. Lämke et al., 2017). In the absence of repeated stressful events, forgetting occurs when the plant activates epigenetic regulatory mechanisms that reset stress memory marks (A. Wibowo et al., 2016). The plant's defense response to individual stressors and their combination during priming and repeated events is expressed in significant modulation of gene expression and the content of various metabolites (A. Aharoni et al., 2011; S.I. Zandalinas et al., 2022). Transcripts and metabolites with a differential response to stress can serve as biomarkers of stress memory (Aina et al., 2024). A characteristic feature of biomarkers (genes, metabolites) is considered to be significant differences in fluctuations in expression (genes) and content (metabolites) during priming, repeated stresses and returns to normal conditions (Y. Ding et al., 2013, 2014; C. Jacques et al., 2021). Putative biomarker genes may be associated with the metabolism of various compounds, including components of plant antioxidant defense, phytohormones, pathogenesis-associated PR proteins, etc. (O.K. Anisimova et al., 2021; S.I. Zandalinas et al., 2022; O. Aina et al., 2024), as well as with the regulation of gene expression (transcription factors, non-coding RNAs, circadian oscillators, etc.) (H. Wei et al., 2022; W. Cao et al., 2024). Based on the presented material, it is assumed that studies of plant defense/adaptive responses, especially cultivated plants, aimed at increasing stress resistance, should be carried out taking into account the aspects discussed in the review. The result of such studies may be the identification of key biomarkers of plant memory about the effects of various stress factors and their combinations, and, as a consequence, the identification of donors of epialleles/epimutations associated with inherited stress memory.
 
Keywords: stress factors, plant stress memory, biomarkers of stress memory.

 

REFERENCES

  1. Villagómez-Aranda A.L., Feregrino-Pérez A.A., García-Ortega L.F., González-Chavira M.M., Torres-Pacheco I., Guevara-González R.G. Activating stress memory: eustressors as potential tools for plant breeding. Plant Cell Reports, 2022, 41(70): 1481-1498 CrossRef
  2. Chen Z.H., Soltis D.E. Evolution of environmental stress responses in plants. Plant Cell Environment, 2020, 43(12): 2827-2831 CrossRef
  3. Siqueira J.A., Batista-Silva W., Zsögön A., Fernie A.R., Araújo W.L., Nunes-Nesi A. Plant domestication: setting biological clocks. Trends in Plant Science, 2023, 28(5): 597-608 CrossRef
  4. Weinhold A. Transgenerational stress-adaption: an opportunity for ecological epigenetics. Plant Cell Reports, 2018, 37(1): 3-9 CrossRef
  5. Zandalinas S.I., Fritschi F.B., Mittler R. Signal transduction networks during stress combination. Journal of Experimental Botany, 2020, 71(5): 1734-1741 CrossRef
  6. Matyssek R., Le Thiec D., Löw M., Dizengremel P., Nunn A.J., Häberle K.H. Interactions between drought and O3 stress in forest trees. Plant Biology (Stuttg.), 2006, 8(1): 11-17 CrossRef
  7. Suzuki N., Rivero R.M., Shulaev V., Blumwald E., Mittler R. Abiotic and biotic stress combinations. New Phytologist, 2014, 203(1): 32-43 CrossRef
  8. Rasmussen S., Barah P., Suarez-Rodriguez M.C., Bressendorff S., Friis P., Costantino P., Bones A.M., Nielsen H.B., Mundy J. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiology, 2013, 161(4): 1783-1794 CrossRef
  9. Zandalinas S.I., Balfagón D., Gómez-Cadenas A., Mittler R. Plant responses to climate change: metabolic changes under combined abiotic stresses. Journal of Experimental Botany, 2022, 73(11): 3339-3354 CrossRef
  10. Aharoni A., Galili G. Metabolic engineering of the plant primary-secondary metabolism interface. Current Opinion in Biotechnology, 2011, 22(2): 239-244 CrossRef
  11. Obata T., Witt S., Lisec J., Palacios-Rojas N., Florez-Sarasa I., Yousfi S., Araus J.L., Cairns J.E., Fernie A.R. Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiology, 2015, 169(4): 2665-2683 CrossRef
  12. Thalmann M., Santelia D. Starch as a determinant of plant fitness under abiotic stress. New Phytologist, 2017, 214(3): 943-951 CrossRef
  13. Heinemann B., Hildebrandt T.M. The role of amino acid metabolism in signaling and metabolic adaptation to stress-induced energy deficiency in plants. Journal of Experimental Botany, 2021, 72(13): 4634-4645 CrossRef
  14. Nair A.U., Bhukya D.P.N., Sunkar R., Chavali S., Allu A.D. Molecular basis of priming-induced acquired tolerance to multiple abiotic stresses in plants. Journal of Experimental Botany, 2022, 73(11): 3355-3371 CrossRef
  15. Salam U., Ullah S., Tang Z.H., Elateeq A.A., Khan Y., Khan J., Khan A., Ali S. Plant metabolomics: an overview of the role of primary and secondary metabolites against different environmental stress factors. Life (Basel), 2023, 13(3): 706 CrossRef
  16. Verma V., Ravindran P., Kumar P.P. Plant hormone-mediated regulation of stress responses. BMC Plant Biology, 2016, 16: 86 CrossRef
  17. Suzuki N., Bassil E., Hamilton J.S., Inupakutika M.A., Zandalinas S.I., Tripathy D., Luo Y., Dion E., Fukui G., Kumazaki A., Nakano R., Rivero R.M., Verbeck G.F., Azad R.K., Blumwald E., Mittler R. ABA is required for plant acclimation to a combination of salt and heat stress. PLoS ONE, 2016, 11(1): e0147625 CrossRef
  18. Devireddy A.R., Arbogast J., Mittler R. Coordinated and rapid whole-plant systemic stomatal responses. New Phytologist, 2020, 225(1): 21-25 CrossRef
  19. Saijo Y., Loo E.P. Plant immunity in signal integration between biotic and abiotic stress responses. New Phytologist, 2020, 225(1): 87-104 CrossRef
  20. Peck S., Mittler R. Plant signaling in biotic and abiotic stress. Journal of Experimental Botany, 2020, 71(5): 1649-1651 CrossRef
  21. Wang X.R., Shao Y., Wang C., Liu Y.Q. Effects of heat stress on virus transmission and virus-mediated apoptosis in whitefly Bemisia tabaci. Archives of Insect Biochemistry and Physiology, 2022, 110(1): e21857 CrossRef
  22. Bai Y., Kissoudis C., Yan Z., Visser R.G.F., van der Linden G. Plant behaviour under combined stress: tomato responses to combined salinity and pathogen stress. The Plant Journal, 2018, 93(4): 781-793 CrossRef
  23. Bostock R.M., Pye M.F., Roubtsova T.V. Predisposition in plant disease: exploiting the nexus in abiotic and biotic stress perception and response. AnnualReviewofPhytopathology, 2014, 52: 517-549 CrossRef
  24. Prasch C.M., Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiology, 2013, 162(4): 1849-1866 CrossRef
  25. Schenke D., Böttcher C., Scheel D. Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signaling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant, Cell & Environment, 2011, 34(11): 1849-1864 CrossRef
  26. Atkinson N.J., Lilley C.J., Urwin P.E. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiology, 2013, 162(4): 2028-2041 CrossRef
  27. Hacquard S., Spaepen S., Garrido-Oter R., Schulze-Lefert P. Interplay between innate immunity and the plant microbiota. Annual Review of Phytopathology, 2017, 55: 565-589 CrossRef
  28. Cheng Y.T., Zhang L., He S.Y. Plant-microbe interactions facing environmental challenge. Cell Host & Microbe, 2019, 26(2): 183-192 CrossRef
  29. Pélissier R., Violle C., Morel J.B. Plant immunity: Good fences make good neighbors? Current Opinion in Plant Biology, 2021, 62: 102045 CrossRef
  30. Virlouvet L., Avenson T.J., Du Q., Zhang C., Liu N., Fromm M., Avramova Z., Russo S.E. Dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays. Frontiers in Plant Science, 2018, 9: 1058 CrossRef
  31. Nishad A., Nandi A.K. Recent advances in plant thermomemory. Plant Cell Reports, 2021, 40(1): 19-27 CrossRef
  32. Jacques C., Salon C., Barnard R.L., Vernoud V., Prudent M. Drought stress memory at the plant cycle level: a review. Plants (Basel), 2021, 10(9): 1873 CrossRef
  33. Hilker M., Schwachtje J., Baier M., Balazadeh S., Bäurle I., Geiselhardt S., Hincha D.K., Kunze R., Mueller-Roeber B., Rillig M.C., Rolff J., Romeis T., Schmülling T., Steppuhn A., van Dongen J., Whitcomb S.J., Wurst S., Zuther E., Kopka J. Priming and memory of stress responses in organisms lacking a nervous system. Biological Reviews of the Cambridge Philosophical Society, 2016, 91(4): 1118-1133 CrossRef
  34. Yanchenko A.V., Bukharov A.F., Fedosov A.Yu. Ovoshchi Rossii, 2023, 5: 28-36 CrossRef (in Russ.).
  35. Bera K., Dutta P., Sadhukhan S. Seed priming with non-ionizing physical agents: plant responses and underlying physiological mechanisms. Plant Cell Reports, 2022, 41(1): 53-73 CrossRef
  36. Nile S.H., Thiruvengadam M., Wang Y., Samynathan R., Shariati M.A., Rebezov M., Nile A., Sun M., Venkidasamy B., Xiao J., Kai G. Nano-priming as emerging seed priming technology for sustainable agriculture-recent developments and future perspectives. Journal of Nanobiotechnology, 2022, 20(1): 254 CrossRef
  37. Pazzaglia J., Badalamenti F., Bernardeau-Esteller J., Ruiz J.M., Giacalone V.M., Procaccini G., Marín-Guirao L. Thermo-priming increases heat-stress tolerance in seedlings of the Mediterranean seagrass P. oceanica. The Marine Pollution Bulletin, 2022, 174: 113164 CrossRef
  38. Provera I., Martinez M., Zenone A., Giacalone V.M., D’Anna G., Badalamenti F., Marín-Guirao L., Procaccini G. Exploring priming strategies to improve stress resilience of Posidonia oceanica seedlings. The Marine Pollution Bulletin, 2024, 200: 116057 CrossRef
  39. Zulfiqar F., Nafees M., Chen J., Darras A., Ferrante A., Hancock J.T., Ashraf M., Zaid A., Latif N., Corpas F.J., Altaf M.A., Siddique K.H.M. Chemical priming enhances plant tolerance to salt stress. Frontiers in Plant Sciences, 2022, 13: 946922 CrossRef
  40. Leuendorf J.E., Frank M., Schmülling T. Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress. Scientific Reports, 2020, 10(1): 689 CrossRef
  41. Hannan Parker A., Wilkinson S.W., Ton J. Epigenetics: a catalyst of plant immunity against pathogens. New Phytologist, 2022, 233(1): 66-83 CrossRef
  42. Iwasaki M., Paszkowski J. Epigenetic memory in plants. EMBO Journal, 2014, 33(18): 1987-1998 CrossRef
  43. Lämke J., Bäurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biology, 2017, 18: 124 CrossRef
  44. Wibowo A., Becker C., Marconi G., Durr J., Price J., Hagmann J., Papareddy R., Putra H., Kageyama J., Becker J., Weigel D., Gutierrez-Marcos J. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife, 2016, 5: e13546 CrossRef
  45. Oyoshi K., Katano K., Yunose M., Suzuki N. Memory of 5-min heat stress in Arabidopsis thaliana. Plant Signaling and Behavior, 2020, 15(8): 1778919 CrossRef
  46. van Buer J., Cvetkovic J., Baier M. Cold regulation of plastid ascorbate peroxidases serves as a priming hub controlling ROS signaling in Arabidopsis thaliana. BMC Plant Biology, 2016, 16(1): 163 CrossRef
  47. Zhang Q., Tian Y. Molecular insights into the transgenerational inheritance of stress memory. Journal of Genetics and Genomics, 2022, 49(2): 89-95 CrossRef
  48. Crisp P.A., Ganguly D., Eichten S.R., Borevitz J.O., Pogson B.J. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Science Advances, 2016, 2: e1501340. CrossRef
  49. Hilker M., Schmülling T. Stress priming, memory, and signaling in plants. Plant, Cell & Environment, 2019, 42(3): 753-761 CrossRef
  50. Brukhin V., Albertini E. Epigenetic modifications in plant development and reproduction. Epigenomes, 2021, 5(4): 25 CrossRef
  51. Iwasaki M., Paszkowski J. Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(23): 8547-8552 CrossRef
  52. Thomas D.T.T, Challabathula D., Puthur J.T. UV-B priming of Oryza sativa var. Kanchana seedlings augments its antioxidative potential and gene expression of stress-response proteins under various abiotic stresses. 3 Biotech, 2019, 9(10): 375 CrossRef
  53. Fan J., Xu J., Zhang W., Amee M., Liu D., Chen L. Salt-induced damage is alleviated by short-term pre-cold treatment in Bermuda grass (Cynodon dactylon). Plants (Basel), 2019, 8(9): 347 CrossRef
  54. Gohari G., Alavi Z., Esfandiari E., Panahirad S., Hajihoseinlou S., Fotopoulos V. Interaction between hydrogen peroxide and sodium nitroprusside following chemical priming of Ocimum basilicum L. against salt stress. Physiologia Plantarum, 2020, 168(2): 361-373 CrossRef
  55. Hussain S., Khan F., Hussain H.A., Nie L. Physiological and biochemical mechanisms of seed priming-induced chilling tolerance in rice cultivars. Frontiers in Plant Science, 2016, 7: 116 CrossRef
  56. Goswami A., Banerjee R., Raha S. Mechanisms of plant adaptation/memory in rice seedlings under arsenic and heat stress: expression of heat-shock protein gene HSP70. AoB Plants, 2010, 2010: plq023. CrossRef
  57. Patade V.Y., Khatri D., Manoj K., Kumari M., Ahmed Z. Cold tolerance in thiourea primed capsicum seedlings is associated with transcript regulation of stress responsive genes. Molecular Biology Reports, 2012, 39(12): 10603-10613 CrossRef
  58. Charrier G. Suffer from drought to withstand the cold. Plant Physiology, 2021, 186(1): 208-209 CrossRef
  59. Bittner A., van Buer J., Baier M. Cold priming uncouples light- and cold-regulation of gene expression in Arabidopsis thaliana. BMC Plant Biology, 2020, 20(1): 281 CrossRef
  60. Aina O., Bakare O.O., Fadaka A.O., Keyster M., Klein A. Plant biomarkers as early detection tools in stress management in food crops: a review. Planta, 2024, 259(3): 60 CrossRef
  61. Al-Zahrani H.S., Alharby H.F., Fahad S. Antioxidative defense system, hormones, and metabolite accumulation in different plant parts of two contrasting rice cultivars as influenced by plant growth regulators under heat stress. Frontiers in Plant Science, 2022, 13: 911846 CrossRef
  62. He J., Yao L., Pecoraro L., Liu C., Wang J., Huang L., Gao W. Cold stress regulates accumulation of flavonoids and terpenoids in plants by phytohormone, transcription process, functional enzyme, and epigenetics. Critical Review in Biotechnology, 2023, 43(5): 680-697 CrossRef
  63. Yamamuro C., Zhu J.K., Yang Z. Epigenetic modifications and plant hormone action. Molecular Plant, 2016, 9(1): 57-70 CrossRef
  64. Brenya E., Pervin M., Chen Z.H., Tissue D.T., Johnson S., Braam J., Cazzonelli C.I. Mechanical stress acclimation in plants: Linking hormones and somatic memory to thigmomorphogenesis. Plant, Cell & Environment, 2022, 45(4): 989-1010 CrossRef
  65. Lysenko N.S., Malyshev L.L., Puzansky R.K., Shavarda A.L., Shelenga T.V. Biomarkers for alumotolerance of winter-hardy forms of Triticum aestivum L. from the VIR collection. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2024, 59(1): 116-130 CrossRef
  66. Ding Y., Liu N., Virlouvet L., Riethoven J.J., Fromm M., Avramova Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biology, 2013, 13: 229 CrossRef
  67. Ding Y., Virlouvet L., Liu N., Riethoven J.J., Fromm M., Avramova Z. Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. BMC Plant Biology, 2014, 14: 141 CrossRef
  68. Forestan C., Farinati S., Zambelli F., Pavesi G., Rossi V., Varotto S. Epigenetic signatures of stress adaptation and flowering regulation in response to extended drought and recovery in Zea mays. Plant, Cell & Environment, 2020, 43(1): 55-75 CrossRef
  69. Avramova Z. Transcriptional 'memory' of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant Journal, 2015, 83(1): 149-159 CrossRef
  70. Bäurle I., Trindade I. Chromatin regulation of somatic abiotic stress memory. Journal of Experimental Botany, 2020, 71(17): 5269-5279 CrossRef
  71. Kim Y., Chung Y.S., Lee E., Tripathi P., Heo S., Kim K.H. Root response to drought stress in rice (Oryza sativa L.). International Journal of Molecular Sciences, 2020, 21(4): 1513 CrossRef
  72. Sathish P., Vanaja M., Jyothi Lakshmi N., Sarkar B., Vijay Kumar G., Vagheera P., Mohan C.H., Maheswari M. Impact of water deficit stress on traits influencing the drought tolerance and yield of maize (Zea mays L.) genotypes. Plant Physiology Reports, 2022, 27(1): 109-118 CrossRef
  73. Bai Y., Sunarti S., Kissoudis C., Visser R.G.F., van der Linden C.G. The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses. Frontiers in Plant Science, 2018, 9: 801 CrossRef
  74. Habib I., Shahzad K., Rauf M., Ahmad M., Alsamadany H., Fahad S., Saeed N.A. Dehydrin responsive HVA1 driven inducible gene expression enhanced salt and drought tolerance in wheat. Plant Physiology and Biochemistry, 2022, 180: 124-133 CrossRef
  75. Liu T., Chen T., Kan J., Yao Y., Guo D., Yang Y., Ling X., Wang J., Zhang B. The GhMYB36 transcription factor confers resistance to biotic and abiotic stress by enhancing PR1 gene expression in plants. Plant Biotechnology Journal, 2022, 20(4): 722-735 CrossRef
  76. Srivastava R., Kobayashi Y., Koyama H., Sahoo L. Cowpea NAC1/NAC2 transcription factors improve growth and tolerance to drought and heat in transgenic cowpea through combined activation of photosynthetic and antioxidant mechanisms. Journal of Integrative Plant Biology, 2023, 65(1): 25-44 CrossRef
  77. Vasquez-Robinet C., Mane S.P., Ulanov A.V, Watkinson J.I., Stromberg V.K., De Koeyer D., Schafleitner R., Willmot D.B., Bonierbale M., Bohnert H.J., Grene R. Physiological and molecular adaptations to drought in Andean potato genotypes. Journal of Experimental Botany, 2008, 59(8): 2109-2123 CrossRef
  78. Filyushin M.A., Shagdarova B.T., Shchennikova A.V., Il’ina A.V., Kochieva E.Z., Varlamov V.P. Pretreatment with chitosan prevents Fusarium infection and induces the expression of chitinases and β-1, 3-glucanases in garlic (Allium sativum L.). Horticulturae, 2022, 8(5): 383 CrossRef
  79. Filyushin M.A., Anisimova O.K., Kochieva E.Z., Shchennikova A.V. Genome-wide identification and expression of chitinase class I genes in garlic (Allium sativum L.) cultivars resistant and susceptible to Fusarium proliferatum. Plants (Basel), 2021, 10(4): 720 CrossRef
  80. Anisimova O.K., Shchennikova A.V., Kochieva E.Z., Filyushin M.A. Pathogenesis-related genes of PR1, PR2, PR4, and PR5 families are involved in the response to Fusarium infection in garlic (Allium sativum L.). International Journal of Molecular Sciences, 2021, 22(13): 6688 CrossRef
  81. Anisimova O.K., Kochieva E.Z., Shchennikova A.V., Filyushin M.A. Thaumatin-like protein (TLP) genes in garlic (Allium sativum L.): Genome-wide identification, characterization, and expression in response to Fusarium proliferatum infection. Plants (Basel), 2022, 11(6): 748 CrossRef
  82. Filyushin M.A., Anisimova O.K., Shchennikova A.V., Kochieva E.Z. Genome-wide identification, expression, and response to Fusarium infection of the SWEET gene family in garlic (Allium sativum L.). International Journal of Molecular Sciences, 2023, 24(8): 7533 CrossRef
  83. Filyushin M.A., Arkhestova D.H., Kochieva E.Z., Shchennikova A.V. Characteristics of a novel monodehydroascorbate reductase gene in corn (Zea mays L.) and its role in the response to stress. Russian Journal of Plant Physiology, 2024, 71(1): 22 CrossRef
  84. Filyushin M.A., Kochieva E.Z., Shchennikova A.V. ZmDREB2.9 gene in maize (Zea mays L.): Genome-wide identification, characterization, expression, and stress response. Plants (Basel), 2022, 11(2): 3060 CrossRef
  85. Filyushin M.A., Anisimova O.K., Shchennikova A.V., Kochieva E.Z. DREB1 and DREB2 genes in garlic (Allium sativum L.): Genome-wide identification, characterization, and stress response. Plants (Basel), 2023, 12(13): 2538 CrossRef
  86. Xu X., Yuan L., Xie Q. The circadian clock ticks in plant stress responses. Stress Biology, 2022, 2(1): 15 CrossRef
  87. Guadagno C.R., Ewers B.E., Weinig C. Circadian rhythms and redox state in plants: till stress do us part. Frontiers in Plant Science, 2018, 9: 247 CrossRef
  88. Bolouri Moghaddam M.R., Van den Ende W. Sweet immunity in the plant circadian regulatory network. Journal of Experimental Botany, 2013, 64(6): 1439-1449 CrossRef
  89. Kidokoro S., Shinozaki K., Yamaguchi-Shinozaki K. Transcriptional regulatory network of plant cold-stress responses. Trends in Plant Science, 2022, 27(9): 922-935 CrossRef
  90. Mody T., Bonnot T., Nagel D.H. Interaction between the circadian clock and regulators of heat stress responses in plants. Genes (Basel), 2020, 11(2): 156 CrossRef
  91. Xu H., Wang X., Wei J., Zuo Y., Wang L. The regulatory networks of the circadian clock involved in plant adaptation and crop yield. Plants (Basel), 2023, 12(9): 1897 CrossRef
  92. Wei H., Xu H., Su C., Wang X., Wang L. Rice CIRCADIAN CLOCK ASSOCIATED 1 transcriptionally regulates ABA signaling to confer multiple abiotic stress tolerance. Plant Physiology, 2022, 190(2): 1057-1073 CrossRef
  93. Dodd A.N., Love J., Webb A.A. The plant clock shows its metal: circadian regulation of cytosolic free Ca(2+). Trends in Plant Science, 2005, 10(1): 15-21 CrossRef
  94. Qi J., Song C.P., Wang B., Zhou J., Kangasjärvi J., Zhu J.K., Gong Z. Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. Journal of Integrative Plant Biology, 2018, 60(9): 805-826 CrossRef
  95. Agurla S., Gahir S., Munemasa S., Murata Y., Raghavendra A.S. Mechanism of stomatal closure in plants exposed to drought and cold stress. Advances in Experimental Medicine and Biology, 2018, 1081: 215-232 CrossRef
  96. Cao W., Yang L., Zhuang M., Lv H., Wang Y., Zhang Y., Ji J. Plant non-coding RNAs: The new frontier for the regulation of plant development and adaptation to stress. Plant Physiology and Biochemistry, 2024, 208: 108435 CrossRef
  97. Soualiou S., Duan F., Li X., Zhou W. Crop production under cold stress: An understanding of plant responses, acclimation processes, and management strategies. Plant Physiology and Biochemistry, 2022, 190: 47-61 CrossRef
  98. Calone R., Mircea D.M., González-Orenga S., Boscaiu M., Zuzunaga-Rosas J., Barbanti L., Vicente O. Effect of recurrent salt and drought stress treatments on the endangered halophyte Limonium angustebracteatum Erben. Plants (Basel), 2023, 12(1): 191 CrossRef
  99. Sadhukhan A., Prasad S.S., Mitra J., Siddiqui N., Sahoo L., Kobayashi Y., Koyama H. How do plants remember drought? Planta, 2022, 256(1): 7 CrossRef
  100. Shinozaki K., Yamaguchi-Shinozaki K. Functional genomics in plant abiotic stress responses and tolerance: From gene discovery to complex regulatory networks and their application in breeding. Proceedings of the Japan Academy. Series B, Biological Sciences, 2022, 98(8): 470-492 (doi: CrossRef 
  101. Khan S.A., Li M.Z., Wang S.M., Yin H.J. Revisiting the role of plant transcription factors in the battle against abiotic stress. International Journal of Molecular Sciences, 2018, 19(6): 1634 CrossRef
  102. Yang L., Wen K.S., Ruan X., Zhao Y.X., Wei F., Wang Q. Response of plant secondary metabolites to environmental factors. Molecules, 2018, 23(4): 762 CrossRef
  103. Glazko V.I., Kosovsky G.Yu., Glazko T.T. On genocentricity and genomocentricity in basic living systems: microorganisms, plants, animals (review).Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2024, 59(3): 426-445 CrossRef

 

back

 


CONTENTS

 

Full article PDF (Rus)